Jenna Lyons has worked at J.Crew for more than 22 years. That may as well be 22 aeons in an industry where emerging designers, like pro ballplayers and cable-news anchors, rarely stay in one place too long, logging a few years here, a few years there. But that hasn't been so for Lyons, 44, who began at J.Crew as an assistant in menswear and, over two decades, worked her way up to president and executive creative director, having led the brand's epic re-invention from purveyor of barn coats and merino wool sweaters to juggernaut of casual-cool American chic. Though J.Crew isn't a luxury brand on par with, say, Balenciaga (one of her favorites), Lyons has nonetheless cultivated an enormous amount of respect and credibility in the notoriously clubby world of high fashion.

J.Crew, once a Main Street also-ran behind Gap and The Limited, is now one of the hot tickets at New York Fashion Week, this year shown at Lincoln Center and attended by every fashion editor, bold-faced blogger, and style star in town. (Last season, Solange and Beyoncé Knowles showed up; this season, Julianne Moore attended.) Under Lyons' watch, J.Crew is looking to conquer Europe next and will open its first overseas storefront, in London, this fall; seven years ago the label launched Madewell, a hip, lower-cost line that seems tailor-made for the coeds who once represented J.Crew's core audience. And then, of course, there is the first lady, a stalwart J.Crew devotee, who, along with her daughters, sported the label at both presidential inaugurations. "To make the first family feel enough pride in our clothes to wear them on the day that they're going to be photographed over and over again—those pictures are going to be a part of history forever—it's just incredible," Lyons tells me, clearly moved.

But the most telling evidence of her growing clout may well be the epic dust storm her personal life has kicked up. Three years ago when she appeared in a J.Crew catalog painting her son Beckett's toes with hot-pink nail polish, conservative pundits on Fox News decried it as "an attack on masculinity." The flap later made news on The Daily Show, with Jon Stewart dubbing the affair "Toemageddon." But that was only a prelude to what would come later. In 2010, Lyons separated from her husband of nine years, artist Vincent Mazeau, and started seeing Courtney Crangi (sister and business partner of jewelry designer Philip Crangi). The gossip columns went berserk covering the messy split. "It's certainly been challenging," Lyons admits. "Someone once said to me, 'If you believe the good, you have to believe the bad.' So I don't read anything. If you listened to what you read in the press, you'd go insane."

Lyons was raised in Palos Verdes, California, just south of Los Angeles, and her parents divorced when she and her kid brother, Spencer, were young. "I'll never forget standing in the grocery store and having to make choices about what to put in the cart. I could feel the stress that [my mother] felt, having to take care of us," Lyons recalls. There were more personal challenges, too. Tall and gangly, she had trouble finding clothes that fit her frame (she stands at six feet today), and a genetic disorder called incontinentia pigmenti gave her bald spots and malformed teeth, for which she still wears dentures.

She eventually moved to New York to attend Parsons School of Design, and after graduating in 1989, took her sketches to Emily Woods, cofounder of J.Crew, then a catalog-driven outpost known for its campus-friendly preppy apparel. She was hired on the spot. As J.Crew grew, Lyons took on more roles, ultimately designing for virtually every division in the company, including lingerie, kidswear, and bath and body. "Things were swelling up underneath me," Lyons says of that period, "and I was always sitting on the raft. I ended up having insane opportunities over time."

Lyons is empathetic that her success has been years in the making. "There's this idea that everybody has to have everything right away. But you have to let the slow burn happen," she says. This is particularly true in fashion, she adds, where there's increasing pressure to hit the big time fast, like Proenza Schouler, the New York–based design duo who had their very first collection picked up by Barneys, and fashion blogger Tavi Gevenson, front row at Prada at age 13. "Those people are incredibly special. The fact of the matter is, I wasn't. I wasn't the superstar. I had to work for it. Really long hours. I didn't have any friends."

In 2003, Millard "Mickey" Drexler, the former CEO of Gap widely credited for turning that label into an American classic, took the helm of J.Crew. Drexler wanted to upgrade the brand and give it more cultural resonance—better designers with better designs, higher-quality materials, more color and vivacity. He gave Lyons, then the newly installed creative director, wide berth to execute his vision. "When someone trusts you that much, ultimately what happens is you won't want to fail. You work harder because you don't want to disappoint," she says.

While Lyons doesn't design anymore, her imprimatur is everywhere. For each of the six core divisions—J.Crew women's, men's, kids, bridal, Madewell, and J.Crew Factory—Lyons approves each outfit before it's shot for the catalogs. (There are several shoots a day, nearly every day of the year.) She has a hand in store locations and decor, the Web design, themes and locations for catalog shoots, and even the labels on the clothes. She's an open-door-policy kind of boss who tore down a wall in her office so her designers can hold up something for her to look at, even when she's in the middle of meetings. Since 2008, she has appeared in J.Crew catalogs, a move that helped nurture her celebrity, first among J.Crew's fans and soon after among style bloggers who'd seized upon her eclectic flair—the Clark Kent glasses and inspired mix-and-matching. Her own style is emblematic of the brand's: daring without being intimidating.

Yet despite J.Crew's tremendous success, Lyons is committed to its affordability. She is nothing if not accessible and democratic, a style icon for the digital era. "I just don't want people to feel like you have to live a certain way to have access to the brand. It's not who we are. I certainly didn't grow up that way. If you did, awesome, more power to you. You can afford to buy anything you want," she says. "Hopefully, you'll buy us, too."

STAY TRUE TO YOUR VALUES: "I don't want people to feel they have to live a certain way to have access to the brand. I certainly didn't grow up that way."

BIG BREAKS COME DURING MOMENTS OF FLUX : Lyons designed for virtually every division at J.Crew. "Things were swelling up underneath me, and I was always sitting on the raft. I ended up having insane opportunities."

THERE'S NO SUCH THING AS OVERNIGHT SUCCESS: "There's this idea that everybody has to have everything right away. But you have to let the slow burn happen. I wasn't the superstar. I had to work for it. Really long hours."

ALLY WITH SUPERIORS WHO RESPECT YOUR TALENTS: Lyons instantly clicked with J.Crew CEO Mickey Drexler. "When someone trusts you that much, ultimately what happens is you won't want to fail."